Russulaceae


The Russulaceae are a diverse family of fungi in the order Russulales, with roughly 1,900 known species and a worldwide distribution. They comprise the brittlegills and the milk-caps, well-known mushroom-forming fungi that include some edible species. These gilled mushrooms are characterised by the brittle flesh of their fruitbodies.
In addition to these typical agaricoid forms, the family contains species with fruitbodies that are laterally striped, closed, or crust-like. Molecular phylogenetics has demonstrated close affinities between species with very different fruitbody types and has discovered new, distinct lineages.
An important group of root-symbiotic ectomycorrhizal fungi in forests and shrublands around the world includes Lactifluus, Multifurca, Russula, and Lactarius. The crust-forming genera Boidinia, Gloeopeniophorella, and Pseudoxenasma, all wood-decay fungi, have basal positions in the family.

Taxonomy

The family Russulaceae was first validly named in 1907 by Dutch botanist Johannes Paulus Lotsy, who included three genera: Russula, Lactarius, and Russulina. He emphasised features such as the granular flesh, thick gills, spiny spores, and milky hyphae and rounded cells. A prior usage of "Russulariées" by French mycologist Ernst Roze in 1876 is not considered a valid publication, since the proper Latin termination for the family rank specified in article 18.4 of the nomenclature code was not used.
Synonyms of Russulaceae include: Ernst Albert Gäumann's Lactariaceae, Fernand Moreau's Asterosporaceae, and David Pegler and Thomas Young's Elasmomycetaceae. The latter family was proposed to contain species with statismosporic and symmetric spores, including the gasteroid genera Elasmomyces, Gymnomyces, Martellia, and Zelleromyces. Calonge and Martín reduced the Elasmomycetaceae to synonymy with the Russulaceae when molecular analysis confirmed the close genetic relationship between the gasteroid and agaricoid genera.

Placement of the family

Historically, the gilled mushrooms of the family Russulaceae were classified with other gilled species in the order Agaricales, but microscopical studies of spore and fruitbody flesh features raised the possibility that they were more closely related with certain "lower fungi" presenting nongilled, crust-like fruitbodies. The use of molecular phylogenetics confirmed that these morphologically diverse fungi form a distinct lineage, first termed the "russuloid clade" and today classified as order Russulales in the class Agaricomycetes. The family's sister group within the order appears to be the crust-like Gloeocystidiellaceae.

Internal systematics

A 2008 molecular phylogenetic study clarified the relationships among the mushroom-forming species of the family. The authors demonstrated the existence of four distinct lineages of gilled mushrooms, which led to the description of Multifurca as a new genus separated from Russula and the segregation of Lactifluus from Lactarius.
Genera with closed fruitbodies within the family are form taxa instead of natural groups: Arcangeliella, Gastrolactarius, and Zelleromyces are phylogenetically part of Lactarius, while Cystangium, Elasmomyces, Gymnomyces, Macowanites, and Martellia belong to Russula. Nevertheless, some of these genus names are still in use, as many of the concerned species have not yet formally been synonymised with Lactarius or Russula.
The crust-like genera Boidinia, Gloeopeniophorella, and Pseudoxenasma, formerly placed in the Corticiaceae or Gloeocystidiellaceae, are now classified in the Russulaceae and basal to the clade of mushroom-forming species described above. Studies have so far failed to clearly circumscribe and place these genera within the family. Boidinia in its current extent is polyphyletic, with some species not falling into the Russulaceae.

Species diversity

Altogether, the Russulaceae comprise around 1,900 accepted species. Russula is by far the largest genus with c. 1,100 species, Lactarius has c. 550, Lactifluus c. 120, Boidinia 13, Multifurca 6, Gloeopeniophorella 6, and Pseudoxenasma 1 species. Closed-fruitbody species not yet synonymised with Lactarius or Russula account for some 150 species.
New species in the Russulaceae continue to be described from various regions, such as the US, Guyana, Brazil, Patagonia, Togo, Sri Lanka, or Thailand. It has been estimated that the real number of Russula species in North America alone might be as high as 2000. Cryptic species may increase true diversity: some morphologically well-defined species, especially in Lactifluus, have been shown to actually encompass several phylogenetic species.

Description

Macroscopic characteristics

Three major types of fruitbodies occur in the Russulaceae: agaricoid and pleurotoid forms with a cap, gills, and a stipe; forms with closed or partially closed fruitbodies, and corticioid, crust-like forms.
The agaricoid species in Lactarius, Lactifluus, Multifurca, and Russula are readily distinguished from other gilled mushrooms by the consistency of their flesh, which is granular, brittle and breaks easily, somewhat like a piece of chalk. Russulaceae never have a volva, but a partial veil can be found in some tropical species. Gills are adnate to decurrent, and the colour of the spore print ranges from white to ochre or orange.
Caps can be dull to very colourful, the latter especially in Russula; their size ranges from 17 mm diameter or less in Russula campinensis to in Lactifluus vellereus. Concentrically ringed caps occur in all Multifurca and several Lactarius species. Laterally striped fruitbodies exist in some, mainly tropical Lactifluus and Russula species. Taste is a distinguishing characteristic in many species, from mild to very acrid. A conspicuous feature of the "milk-caps" in Lactarius, Lactifluus, and Multifurca furcata is the latex or "milk" their fruitbodies exude when bruised.
The secotioid and gasteroid species in Lactarius and Russula are derived from agaricoid forms. Secotioid species still have a stipe but the cap does not open fully, while in gasteroid species, fruitbodies are completely closed and the stipe is reduced; in both cases, the spore-bearing structure is made up of convoluted gills that are more or less crowded and anastomosed. These closed-fruitbody species represent a continuum of secotioid to gasteroid, above-ground to below-ground fruitbodies, with spores forcibly discharged or not. Secotioid or gasteroid Lactarius exude latex just like their agaricoid relatives.
The corticioid species of Boidinia, Gloeopeniophorella, and Pseudoxenasma develop crust-like fruitbodies with a smooth, porous, or flaky surface and grow on tree logs or dead branches.

Microscopic characteristics

All Russulaceae, including the corticioid species, are characterised by spherical to elliptic basidiospores with a faint to very distinct ornamentation that stains bluish-black with Melzer's reagent. Basidia are usually club-shaped and four-spored. Russulaceae species do not have clamp connections.
Characteristic cells with an oily content are found in the hymenium. In Russulaceae, these show a positive colour reaction when treated with sulfoaldehydes. They are also present in the hyphal sheath of ectomycorrhizal roots colonised by Russulaceae.
The feature responsible for the brittle fruitbody structure in the mushroom-forming species are globular cells, called sphaerocytes or sphaerocysts, that compose the flesh alongside the usual hyphae. Sometimes, these cells are clustered, and the position and arrangement of these clusters differs among genera.
Another particular trama cell type are lactiferous hyphae. These are hyphae carrying the "milk" or "latex" exuded by the milk-caps; they react positively with sulfoaldehydes, form an abundantly branched system in the trama and end as pseudocystidia in the hymenium. In general, only Lactarius, Lactifluus and Multifurca furcata possess lactifers. In Russula, similar hyphae can sometimes be observed in the trama, but these are not as abundantly branched as real lactifers and do not extend into the hymenium as pseudocystidia. This traditional distinction line between the "milk-caps" and Russula is however less evident in some tropical species presenting intermediate states.

Genera distinction

Some characteristics of the mushroom-forming genera can be less obvious or absent in tropical species. Distinguishing between Lactarius and Lactifluus based on morphology alone is quite difficult, as clear synapomorphies for both genera have yet to be identified. Most field guides treat the two genera together, often because Lactifluus is not yet recognised as a separate genus.
  • Boidinia: corticioid; loose texture; surface smooth, with pores, or flaky; spores spherical with spiny to warty ornamentation. Note that the genus is polyphyletic and needs to be redefined.
  • Gloeopeniophorella: corticioid; surface almost smooth; hyphae without clamp connections; thick-walled cystidia and gloeocystidia present; spores with wrinkled ornamentation.
  • Lactarius: agaricoid or gasteroid; exuding latex*; caps sometimes zonate, viscose or glutinate, but never annulate; rarely thick-walled cells in cuticles of the cap and the stipe and sphaerocytes in the gills.
  • Lactifluus: agaricoid or pleurotoid; exuding latex*; caps never zonate, viscose or glutinate, but sometimes annulate; thick-walled cells in cap and stipe cuticles; often sphaerocytes in the gill trama.
  • Multifurca: agaricoid; caps zonate ; gills regularly forked; only M. furcata exuding latex; spore print orange; spores very small; microscopical trama and hymenium features very variable.
  • Pseudoxenasma: corticioid; wax-like texture; gloeocystidia with spherical apical appendices; basidia developing laterally on hyphae ; spores broadly ellipsoid to roughly spherical, with warty ornamentation.
  • Russula: agaricoid, gasteroid or pleurotoid; never exuding latex; caps often brightly coloured with stipe and gills much paler; caps not zonate*; spore print white, cream, ochre, or orange; no true lactiferous hyphae*; sphaerocytes abundant in gill, cap, and stipe trama.